| Legend |
|---|
| Justification for qualification based on EPPO PM 4 Standards |
| Justification for disqualification |
| Additional or non-conclusive information |
| Standard text |
NAME OF THE ORGANISM: Nepovirus nigranuli (tomato black ring virus) {Tomato black ring nepovirus} (TBRV00)
GENERAL INFORMATION ON THE PEST
Name as submitted in the project specification (if different):
Tomato black ring nepovirus
Pest category:
Viruses and viroids
1- Identity of the pest/Level of taxonomic listing:
Is the organism clearly a single taxonomic entity and can it be adequately distinguished from other entities of the same rank?
Yes
Is the pest defined at the species level or lower?:
Yes
Can listing of the pest at a taxonomic level higher than species be supported by scientific reasons or can species be identified within the taxonomic rank which are the (main) pests of concern?
- Not relevant: Fruits (including hops) sector
If necessary, please list the species:
-
Is it justified that the pest is listed at a taxonomic rank below species level?
Not relevant
Conclusion:
- Candidate: Fruits (including hops) sector
Justification (if necessary):
Tomato black ring virus (TBRV) was first reported in the UK (Smith, 1946). Although early studies first described TBRV and beet ringspot virus (BRSV) as distinct viruses (Harrison, 1957, 1958), soon afterwards they were considered serologically distinct strains of TBRV (Murant, 1970). More recently, the International Committee on Taxonomy of Viruses (ICTV) recognized them as closely related but distinct members of the genus Nepovirus (family Secoviridae) subgroup B (Pringle, 1998): tomato black ring (TBRV, Nepovirus nigranuli) and beet ringspot virus (BRSV, Scottish beet ringspot isolate of TBRV (TBRV-S), Nepovirus betae).
2 – Status in the EU:
Is this pest already a quarantine pest for the whole EU?
No
Presence in the EU:
Yes
List of countries (EPPO Global Database):
Belgium (2017); Bulgaria (2002); Croatia (2002); Czech Republic (1994); Finland (2011); France (1992); Germany (1993); Greece (1997); Hungary (1992); Ireland (1993); Lithuania (2021); Netherlands (2022); Poland (2021); Slovakia (2002); Sweden (1993)
Conclusion:
Candidate
Justification (if necessary):
Data of the presence of this pest on the EU territory are available in EPPO Global Database (https://gd.eppo.int/).
HOST PLANT N°1: Fragaria (1FRAG) for the Fruits (including hops) sector.
Origin of the listing:
Commission Implementing Directive (EU) 2014/98/EU and Commission Implementing Regulation (EU) 2019/2072
Plants for planting:
Plants intended for planting, except seeds
3 - Is the pest already listed in a PM4 standard on the concerned host plant?
Yes
Conclusion:
Evaluation continues
Justification (if necessary):
Listed as 'Tomato black ring nepovirus (TBRV)' in EPPO Standard PM 4-11 Certification scheme for strawberry; with testing recommended.
The Fruit SEWG decided to further analyse the data of economic impact available for this pest/host combination. Evaluation continues on this criteria.
The Fruit SEWG decided to further analyse the data of economic impact available for this pest/host combination. Evaluation continues on this criteria.
4 - Are the listed plants for planting the main* pathway for the "pest/host/intended use" combination? (*: significant compared to others):
Conclusion:
Justification:
5 - Economic impact:
Are there documented reports of any economic impact on the host?
No
Justification:
In general very few reports on nepoviruses of berries can be found, most references dating before 1995.
Martin & Tzanetakis (2006) reported that symptoms of tomato black ring virus on Fragaria vesca indicator clones may vary from being asymptomatic to leaf blotching. Symptoms often diminish after the first season, as in the case of RpRSV.
Symptoms in strawberry cultivars are similar to those caused by RpRSV.
The incidence of virus-infected plants generally remains localised because of limited spread by the nematode vectors (EFSA PLH, 2013).
EFSA (2013) refers to Murant & Lister (1987) as part of a general statement on the impact of nepoviruses on Fragaria and Rubus. On checking, this article only relates specifically to RRV and TBRV alone or as a mixed infection on strawberry, and even then it states "with large outbreaks economic loss may...be considerable", and then proceeds to describe symptoms rather than economic impacts in sensu stricto.
Martin & Tzanetakis (2006) reported that symptoms of tomato black ring virus on Fragaria vesca indicator clones may vary from being asymptomatic to leaf blotching. Symptoms often diminish after the first season, as in the case of RpRSV.
Symptoms in strawberry cultivars are similar to those caused by RpRSV.
The incidence of virus-infected plants generally remains localised because of limited spread by the nematode vectors (EFSA PLH, 2013).
EFSA (2013) refers to Murant & Lister (1987) as part of a general statement on the impact of nepoviruses on Fragaria and Rubus. On checking, this article only relates specifically to RRV and TBRV alone or as a mixed infection on strawberry, and even then it states "with large outbreaks economic loss may...be considerable", and then proceeds to describe symptoms rather than economic impacts in sensu stricto.
What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
Is the economic impact due to the presence of the pest on the named host plant for planting, acceptable to the propagation and end user sectors concerned?
Is there unacceptable economic impact caused to other hosts (or the same host with a different intended use) produced at the same place of production due to the transfer of the pest from the named host plant for planting?
No
Conclusion:
Not candidate
Justification:
Cultivation practices strongly limit this potential for impact. According to EFSA (2013), the most significant factor is certainly that efficient voluntary certification schemes for strawberry and raspberry are in place and ensure that healthy planting materials are used by growers. Additional factors contributing to a reduction of the impact are (1) the significantly shorter cycles of modern strawberry and raspberry cultivation practices (one to two seasons), which limit the potential for disease build-up, (2) the increasingly frequent use of soil-less cultivation practices, which limit the impact of nematode vectors and (3) the availability of resistant or tolerant cultivars of raspberry. As a consequence of the conjunction of these various factors, these nematode-transmitted viruses are found only occasionally in these crops and the diseases they cause are considered of minor significance by growers as illustrated during the hearing of industry experts. Current impact of these viruses (under existing regulatory framework) in Fragaria, Rubus and Ribes hosts was considered by EFSA (2013) to be minimal to minor, with low uncertainty.
The Fruit SEWG commented that voluntary certification schemes are not widely used in all EU countries. For instance, in Spain, between 60-70% of the material is certified in Fragaria, and practically nothing in Rubus and Ribes (certification started in 2024). Consequently, in absence of evidence for relevant symptoms and economic impact in the last decades, the Fruit SEWG concluded that economic impact should be considered as acceptable.
The Fruit SEWG commented that voluntary certification schemes are not widely used in all EU countries. For instance, in Spain, between 60-70% of the material is certified in Fragaria, and practically nothing in Rubus and Ribes (certification started in 2024). Consequently, in absence of evidence for relevant symptoms and economic impact in the last decades, the Fruit SEWG concluded that economic impact should be considered as acceptable.
6 - Are there feasible and effective measures available to prevent the presence of the pest on the plants for planting at an incidence above a certain threshold (including zero) to avoid an unacceptable economic impact as regards the relevant host plants?
Conclusion:
Justification:
7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
Conclusion:
Justification:
CONCLUSION ON THE STATUS:
Disqualified: no economic impact reported in the last decade.
8 - Tolerance level:
Is there a need to change the Tolerance level:
Yes
Proposed Tolerance levels:
Delisting
9 - Risk management measures:
Is there a need to change the Risk management measure:
Yes
Proposed Risk management measure:
Delisting
REFERENCES:
- EFSA (2013) EFSA Panel on Plant Health (PLH). Scientific opinion on the risk to plant health posed by Arabis mosaic virus, Raspberry ringspot virus, Strawberry latent ringspot virus and Tomato blackring virus to the EU territory with the identification and evaluation of risk reduction options. EFSA Journal 11(10), 3377. Available at https://efsa.onlinelibrary.wiley.com/doi/epdf/10.2903/j.efsa.2013.3377.
- Martin RR & Tzanetakis IE (2006) Characterization and recent advances in detection of strawberry viruses. Plant disease 90(4). DOI: 10.1094/PD-90-0384.
- Murant & Lister (1987) Nematode-borne diseases. European nepoviruses in strawberry. 46-52. In Converse (1987). Virus Disease of Small Fruits. University of Nebraska - Lincoln. Available at https://digitalcommons.unl.edu/cgi/viewcontent.cgi?article=1394&context=bioscifacpub
HOST PLANT N°2: Prunus avium (PRNAV) for the Fruits (including hops) sector.
Origin of the listing:
Commission Implementing Directive (EU) 2014/98/EU and Commission Implementing Regulation (EU) 2019/2072
Plants for planting:
Plants intended for planting, except seeds
3 - Is the pest already listed in a PM4 standard on the concerned host plant?
Yes
Conclusion:
Evaluation continues
Justification (if necessary):
Listed as 'Tomato black ring nepovirus (TBRV)' in EPPO Standard PM 4-29 Certification scheme for cherry; with testing recommended. However, in the responses to the questionnaire, CZ and PL supported deregulation. CZ considered that economic impact was acceptable for stone fruit species in CZ. PL conconsidered that plants for planting was not the main pathway. Evaluation continues on these criteria.
Remark: The assessment performed covers the given host species as well as interspecific hybrids with other Prunus species.
Remark: The assessment performed covers the given host species as well as interspecific hybrids with other Prunus species.
4 - Are the listed plants for planting the main* pathway for the "pest/host/intended use" combination? (*: significant compared to others):
Yes
Conclusion:
Candidate
Justification:
Tomato black ring virus (TBRV) is a European nepovirus with a wide host range. It infects naturally many species of wild and cultivated monocotyledonous and dicotyledonous plants. Nearly all commonly used herbaceous test plants are susceptible (Murrant, 1970; Hasiów-Jaroszewska & Zarzyńska-Nowak, 2022). The virus has been reported in Prunus avium and P. cerasus (Pavliuk et al., 2020).
TBRV is vectored by free-living soil-inhabiting nematodes of the genus Longidorus, it is transmitted most efficiently by L. attenuatus (Harrison, 1964). Various populations of L. attenuatus can vary in their efficiency to transmit TBRV (Brown et al., 1989). The closely related beet ringspot virus is transmitted by L. elongatus (Harrison et al, 1961), and L. elongatus is also able to transmit TBRV (Taylor & Murrant, 1969). Both larvae and adult nematodes transmit the virus, but the virus does not multiply in the vector, and it is not retained after moulting, nor is it passed to nematode progeny. L. elongatus kept in fallow soil retains infectivity up to about 9 weeks (Murrant, 1970; Hasiów-Jaroszewska & Zarzyńska-Nowak, 2022).
TBRV can be introduced by infected plant material. Several countries have intercepted TBRV or traced a new national record of TBRV to imported plant material that was infected with TBRV, e.g. in Canada TBRV-infected grapevine was detected, in Brazil TBRV-infected seed potatoes were found, both were imported from Europe (Stobbs & Van Schagen, 1984; Kudamatsu et al., 1981).
TBRV is reported to be seed transmitted in at least twenty-four plant species in fifteen botanical families. In many hosts more than 10%, and in some 100%, of progeny seedlings are infected. Many plants infected through the seed show no symptoms. Virus was transmitted to seed of raspberry and strawberry from either male or female parent, but plants pollinated with virus-carrying pollen did not become infected (Lister & Murant, 1967).
TBRV is vectored by free-living soil-inhabiting nematodes of the genus Longidorus, it is transmitted most efficiently by L. attenuatus (Harrison, 1964). Various populations of L. attenuatus can vary in their efficiency to transmit TBRV (Brown et al., 1989). The closely related beet ringspot virus is transmitted by L. elongatus (Harrison et al, 1961), and L. elongatus is also able to transmit TBRV (Taylor & Murrant, 1969). Both larvae and adult nematodes transmit the virus, but the virus does not multiply in the vector, and it is not retained after moulting, nor is it passed to nematode progeny. L. elongatus kept in fallow soil retains infectivity up to about 9 weeks (Murrant, 1970; Hasiów-Jaroszewska & Zarzyńska-Nowak, 2022).
TBRV can be introduced by infected plant material. Several countries have intercepted TBRV or traced a new national record of TBRV to imported plant material that was infected with TBRV, e.g. in Canada TBRV-infected grapevine was detected, in Brazil TBRV-infected seed potatoes were found, both were imported from Europe (Stobbs & Van Schagen, 1984; Kudamatsu et al., 1981).
TBRV is reported to be seed transmitted in at least twenty-four plant species in fifteen botanical families. In many hosts more than 10%, and in some 100%, of progeny seedlings are infected. Many plants infected through the seed show no symptoms. Virus was transmitted to seed of raspberry and strawberry from either male or female parent, but plants pollinated with virus-carrying pollen did not become infected (Lister & Murant, 1967).
5 - Economic impact:
Are there documented reports of any economic impact on the host?
No
Justification:
No specific reports on symptom development of TBRV in Prunus avium.
What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
Is the economic impact due to the presence of the pest on the named host plant for planting, acceptable to the propagation and end user sectors concerned?
Is there unacceptable economic impact caused to other hosts (or the same host with a different intended use) produced at the same place of production due to the transfer of the pest from the named host plant for planting?
No
Conclusion:
Not candidate
Justification:
6 - Are there feasible and effective measures available to prevent the presence of the pest on the plants for planting at an incidence above a certain threshold (including zero) to avoid an unacceptable economic impact as regards the relevant host plants?
Conclusion:
Justification:
As other nepoviruses
7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
Conclusion:
Justification:
CONCLUSION ON THE STATUS:
Disqualified: no report of economic impact on this host.
8 - Tolerance level:
Is there a need to change the Tolerance level:
Yes
Proposed Tolerance levels:
Delisting
9 - Risk management measures:
Is there a need to change the Risk management measure:
Yes
Proposed Risk management measure:
Delisting
REFERENCES:
- Brown DJF, Murant AF & Trudgill DL (1989) Differences between isolates of the English serotype of tomato black ring virus in their transmissibility by an English population of Longidorus attenuatus (Nematoda: Dorylaimoidea). Revue de Nématologie 12(1), 51-56.
- Fowkes A, Adams IP, Jones RAC, Fox A, McGreig S & Boonham N (2021) Historical and recent tomato black ring virus and beet ringspot virus isolate genomes reveal interspecies recombination and plant health regulation inconsistencies. Plant Pathology 71(3), 729-740.
- Harrison BD (1957) Soil transmission of Beet ringspot virus to peach (Prunus persica). Nature 180, 1055–1056.
- Harrison BD (1957) Studies on the host range, properties and mode of transmission of beet ringspot virus. Annals of Applied Biology 45, 462-472.
- Harrison BD (1958) Relationship between beet ringspot, potato bouquet and tomato black ring viruses. Journal of General Microbiology 18, 450–460.
- Harrison BD (1964) Specific nematode vectors for serologically distinctive forms of raspberry ringspot and tomato black ring viruses. Virology 22, 544-550. doi: 10.1016/0042-6822(64)90075-3. PMID: 14166114.
- Harrison BD, Mowat WP & Taylor CE (1961) Transmission of a strain of tomato black ring virus by Longidorus elongatus (Nematoda). Virology 14, 480-485. doi: 10.1016/0042-6822(61)90341-5. PMID: 13711805.
- Hasiów-Jaroszewska B & Zarzyńska-Nowak A (2022) Tomato black ring virus (ring spot of beet). CABI Compendium. https://doi.org/10.1079/cabicompendium.54060.
- Kudamatsu M, Barradas MM & Alba APC (1981) Characterization of the “bouquet” strain of tomato black ring virus from imported seed-potato in Brazil. Turrialba 31(3), 195 – 200.
- Lister RM & Murant AF (1967) Seed-transmission of nematode-borne viruses. Annals of Applied Biology 59(1), 49-62. https://doi.org/10.1111/j.1744-7348.1967.tb04416.x
- Murrant AF (1970) Tomato black ring virus nr. 38. In Description of Plant Viruses (accessed 7/Aug/2024). https://www.dpvweb.net/dpv/showdpv/?dpvno=38
- Pringle CR (1998) Virus taxonomy-San Diego 1998. Archives of Virology 143, 1449–1459.
- Pavliuk L, Udovychenko K, Riaba I & Bublyk M (2021) Detection of sour and sweet cherry viruses in Ukraine. Agronomy Research 19(1), 199–209. https://doi.org/10.15159/AR.20.238
- Stobbs LW & Van Schagen JG (1984) Occurrence of tomato black ring virus on grapevine in southern Ontario. Canadian Plant Disease Survey 64(1), 3-5.
- Taylor CE & Murant AF (1969) Transmission of strains of raspberry ringspot and tomato black ring viruses by Longidorus elongatus (de Man). Annals of Applied Biology 64(1), 43-48. https://doi.org/10.1111/j.1744-7348.1969.tb02853.x